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Exaiptasia Diaphana from the Great Barrier Reef: a Valuable Resource for Coral 2 Symbiosis Research

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Exaiptasia Diaphana from the Great Barrier Reef: a Valuable Resource for Coral 2 Symbiosis Research bioRxiv preprint doi: https://doi.org/10.1101/775510; this version posted September 20, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 Exaiptasia diaphana from the Great Barrier Reef: a valuable resource for coral 2 symbiosis research 3 4 Authors and Affiliations: 5 Dungan, Ashley M.1*§, Hartman, Leon1,2§, Tortorelli, Giada1, Belderok, Roy1,3, Lamb, 6 Annika M.1,4, Pisan, Lynn1,5, McFadden, Geoffrey I.1, Blackall, Linda L.1, van Oppen, 7 Madeleine J. H.1,4 8 1School of Biosciences, University of Melbourne, Melbourne, VIC, Australia 9 2 Swinburne University of Technology, Hawthorn, VIC, Australia 10 3 Department of Freshwater and Marine Ecology, Institute for Biodiversity and Ecosystem 11 Dynamics, University of Amsterdam, Amsterdam, The Netherlands 12 4 Australian Institute of Marine Science, Townsville, QLD, Australia 13 5 Kantonsschule Zug, Zug, Switzerland 14 15 §Equal first authors 16 *Correspondence: 17 Ashley M. Dungan 18 [email protected] 19 Mobile: +61 403 442 289 20 ORCID: 0000-0003-0958-2177 21 22 Keywords: symbiosis, Exaiptasia diaphana, Exaiptasia pallida, model system, physiology, 23 Symbiodiniaceae bioRxiv preprint doi: https://doi.org/10.1101/775510; this version posted September 20, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 24 Abstract 25 The sea anemone, Exaiptasia diaphana, commonly known as Exaiptasia pallida or Aiptasia 26 pallida, has become increasingly popular as a model for cnidarian-microbiome symbiosis 27 studies due to its relatively rapid growth, ability to reproduce sexually and asexually, and 28 symbiosis with diverse prokaryotes and the same microalgal symbionts (family 29 Symbiodiniaceae) as its coral relatives. Clonal E. diaphana strains from Hawaii, the Atlantic 30 Ocean, and Red Sea are now established for use in research. Here, we introduce Great Barrier 31 Reef (GBR)-sourced E. diaphana strains as additions to the model repertoire. Sequencing of 32 the 18S rRNA gene confirmed the anemones to be E. diaphana while genome-wide single 33 nucleotide polymorphism analysis revealed four distinct genotypes. Based on Exaiptasia- 34 specific inter-simple sequence repeat (ISSR)-derived sequence characterized amplified region 35 (SCAR) marker and gene loci data, these four E. diaphana genotypes are distributed across 36 several divergent phylogenetic clades with no clear phylogeographical pattern. The GBR E. 37 diaphana genotypes comprised three females and one male, which all host Breviolum 38 minutum as their homologous Symbiodiniaceae endosymbiont. When acclimating to an 39 increase in light levels from 12 to 28 µmol photons m-2 s-1, the genotypes exhibited 40 significant variation in maximum quantum yield of Symbiodiniaceae photosystem II and 41 Symbiodiniaceae cell density. The comparatively high levels of physiological and genetic 42 variability among GBR anemone genotypes makes these animals representative of global E. 43 diaphana diversity and thus excellent model organisms. The addition of these GBR strains to 44 the worldwide E. diaphana collection will contribute to cnidarian symbiosis research, 45 particularly in relation to the climate resilience of coral reefs. bioRxiv preprint doi: https://doi.org/10.1101/775510; this version posted September 20, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 46 1 Introduction 47 1.1 Coral Reefs 48 The Great Barrier Reef (GBR) contains abundant and diverse biota, including more than 300 49 species of stony corals (Fabricius et al. 2005), making it one of the most unique and complex 50 ecosystems in the world. In addition to its tremendous environmental importance, the GBR’s 51 social and economic value is estimated at $A56 billion, supporting 64,000 jobs and injecting 52 $A6.4 billion into the Australian economy annually (O’Mahony et al. 2017). 53 Coral reef waters are typically oligotrophic, but stony corals thrive in this environment and 54 secrete the calcium carbonate skeletons that create the physical structure of the reef. Corals 55 achieve this through their symbiosis with single-celled algae of the family Symbiodiniaceae 56 that reside within the animal cells and provide the host with most of its energy (Muscatine 57 and Porter 1977). Additional support is provided by communities of prokaryotes, and 58 possibly by other microbes such as viruses, fungi and endolithic algae living in close 59 association with coral. This entity, comprising the host and its microbial partners, is termed 60 the holobiont (Rohwer et al. 2002). During periods of extreme thermal stress, the coral- 61 Symbiodiniaceae relationship breaks down. Stress-induced cellular damage creates a state of 62 physiological dysfunction, which leads to separation of the partners and, potentially, death of 63 the coral animal. This process, ‘coral bleaching’, is a substantial contributor to coral cover 64 loss globally (Baird et al. 2009; De'ath et al. 2012; Eakin et al. 2016; Hughes et al. 2017; 65 Hughes et al. 2018). 66 1.2 Exaiptasia diaphana 67 Model systems are widely used to explore research questions where experimentation on the 68 system of interest has limited feasibility or ethical constraints. Established model systems, 69 such as Drosophila melanogaster and Caenorhabditis elegans, have played crucial roles in 70 the progress of understanding organismal function and evolution in the past 50 years (Davis 71 2004). The coral model Exaiptasia diaphana was formally proposed by Weis et al. (2008) as 72 a useful system to study cnidarian endosymbiosis and has since achieved widespread and 73 successful use. 74 E. diaphana is a small sea anemone (≤60 mm long) found globally within temperate and 75 tropical marine shallow-water environments (Grajales and Rodriguez 2014). Originally 76 positioned taxonomically within the genus Aiptasia, E. diaphana and twelve other Aiptasia bioRxiv preprint doi: https://doi.org/10.1101/775510; this version posted September 20, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 77 species were combined into a new genus, Exaiptasia (Grajales and Rodriguez 2014). 78 Although Exaiptasia pallida was proposed as the taxonomic name for the twelve 79 synonymized species, the International Commission on Zoological Nomenclature (ICZN) 80 ruled against this because the species epithet diaphana (Rapp 1829) predated pallida (Verrill 81 1864) and therefore had precedence according to the Principle of Priority (ICZN 2017). 82 E. diaphana was first used to study cellular regeneration (Blanquet and Lenhoff 1966), with 83 its systematic use in the study of cnidarian-algal symbioses dating back to 1976 when the 84 regulation of in hospite Symbiodiniaceae density was explored (Steele 1976). Since then, 85 studies using E. diaphana have focused on the onset, maintenance, and disruption of 86 symbiosis with Symbiodiniaceae (Belda-Baillie et al. 2002; Fransolet et al. 2014; Bucher et 87 al. 2016; Hillyer et al. 2017; Cziesielski et al. 2018). E. diaphana has also been used in 88 studies of toxicity (Duckworth et al. 2017; Howe et al. 2017), ocean acidification (Hoadley et 89 al. 2015), disease and probiotics (Alagely et al. 2011), and cnidarian development (Chen et 90 al. 2008; Grawunder et al. 2015; Carlisle et al. 2017). Key differences between corals and E. 91 diaphana are the absence of a calcium carbonate skeleton, the constant production of asexual 92 propagates, and the greater ability to survive bleaching events in the latter. These features 93 allow researchers to use E. diaphana to investigate cellular processes that would otherwise be 94 difficult with corals, such as those that require survival post-bleaching to track re- 95 establishment of eukaryotic and prokaryotic symbionts. Further, adult anemones can be fully 96 bleached without eliciting mortality, which is often difficult for corals, thus providing a 97 system for algal reinfection studies independent of sexual reproduction and aposymbiotic 98 larvae. 99 Three strains of E. diaphana currently dominate the research field as models for coral 100 research. H2 (female) was originally collected from Coconut Island, Hawaii, USA (Xiang et 101 al. 2013), CC7 (male) from the South Atlantic Ocean off North Carolina, USA (Sunagawa et 102 al. 2009) and RS (female, pers.comm., but see (Schlesinger et al. 2010)) collected from the 103 Red Sea at Al Lith, Saudia Arabia (Cziesielski et al. 2018). The majority of E. diaphana 104 resources have been developed from the clonal line, CC7, including reproductive studies 105 (Grawunder et al. 2015), transcriptomes (Sunagawa et al. 2009; Lehnert et al. 2012; Lehnert 106 et al. 2014) and an anemone genome sequence (Baumgarten et al. 2015). Prior work 107 evaluating multiple E. diaphana strains has shown variation in sexual reproduction 108 (Grawunder et al. 2015), Symbiodiniaceae specificity (Thornhill et al. 2013; Grawunder et al. bioRxiv preprint doi: https://doi.org/10.1101/775510; this version posted September 20, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 109 2015), and resistance to thermal stress (Bellis and Denver 2017; Cziesielski et al. 2018). 110 However, Australian contributions to these efforts have been hampered as researchers have 111 not had access to the established strains as import permits for alien species are difficult to 112 secure.
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